Suture dehiscence and collagen content in the human mitral and tricuspid annuli

Abstract

Postoperative suture dehiscence is an important mode of short-term mitral and tricuspid valve (MV, TV) repair failure. We sought to evaluate suture pullout forces and collagen density in human atrioventricular valves for a better understanding of the comparative physiology between the valves and the underlying mechanobiological basis for suture retention. Mitral and tricuspid annuli were each excised from hearts from human donors age 60–79 with no history of heart disease (n = 6). Anchor sutures were vertically pulled until tearing through the tissue. Suture pullout force (FP) was measured as the maximum force at dehiscence. Subsequently, tissue samples from each tested suture position were evaluated for collagen content using a standard hydroxyproline assay. Among all mitral positions, no significant differences were detected among positions or regions with mean FP values falling between 6.9 ± 2.6 N (posterior region) and 10.3 ± 4.7 N (anterior region). Among all tricuspid positions, the maximum FP and minimum FP were 24.0 ± 9.2 N (trigonal region) and 4.5 ± 2.6 N (anterior region). Although for the MV, a given sample’s collagen content had no correlation to its corresponding FP, the same relationship was significant for the TV. Further, the TV exhibited comparable FP to the MV overall, despite a nearly 40% reduction in collagen content. These findings suggest that sutures placed in the trigonal region of the TV have higher pullout force than those placed along other segments of the annuli. Furthermore, there are likely differences in collagen orientation between the mitral and tricuspid annuli, such that collagen content strongly impacts FP in one, but not the other.

Notes

Acknowledgements

This study was partially supported by a fellowship from the National Science Foundation (DGE-1148903: ELP) and Grants from the National Heart, Lung and Blood Institute (HL113216, HL127570 and HL 104080). Additionally, Fatiesa Sulejmani is supported by the Georgia Institute of Technology, Emory University, Peking University Global Biomedical Engineering Research and Education Fellowship. The authors wish to thank Tausif Salim for his assistance with collagen quantification.

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The authors declare that they have no conflict of interest.

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Supplementary material

Appendix

Further analysis was carried out to further elucidate the dehiscence mechanism and differences between the atrioventricular annuli. Two additional metrics were computed: total energy required for tissue failure (TERTIF) and full width at half maximum (FWHM). TERTIF was defined as the integral of the force–displacement curve from 5 s prior to failure until failure (to ensure any slackness at initial loading did not influence the analysis). TERTIF was a measure of required loading for tissue failure. FWHM was defined as the duration during which greater than half the pullout force (FP) was applied before and after tissue failure. FWHM may shed light on uniformity of collagen crimp in MV and TV annuli; barring the influence of other factors, e.g., alignment direction, homogeneously crimped collagen fibers should load/break more quickly (lower FWHM), and heterogeneously crimped fibers should load/break more slowly (higher FWHM).

No differences were found in TERTIF between MV and TV annuli (29.1 ± 13.6 vs 33.3 ± 28.6 N mm, p = 0.280). Although the MV annulus showed a trend of lower FWHM compared to the TV annulus, this difference was not significant (6.7 ± 1.8 vs 7.4 ± 2.7 s, p = 0.086). These results allude to a difference in homogeneity in collagen crimp between the two annuli. However, further studies with larger sample sizes are necessary to confirm this hypothesis.

Figure 5 shows a summary of correlation analyses carried out on FWHM and TERTIF. We found a strong positive linear correlation between FWHM and HYP for both wet and dry weights of the TV (r2 = 0.2634, p < 0.001; r2 = 0.2935, p < 0.001), whereas a weak negative relationship was found for the MV (r2 = 0.0787, p = 0.037; r2 = 0.0262, p = 0.237). This suggests that along the TV annulus, in areas with higher collagen content, barring differences in fiber alignment, collagen fibers tend to be less uniformly crimped. Along the MV annulus, this trend is nonexistent and possibly reversed.

Similarly, a strong positive linear correlation was found between TERTIF and HYP for both wet and dry weights of the TV (r2 = 0.6083, p < 0.001; r2 = 0.5779, p < 0.001), and a weak negative relationship was found for the MV (r2 = 0.082, p = 0.034; r2 = 0.0083, p = 0.508). This result indicates that along the TV annulus, positions with higher collagen content required higher energy for tissue dehiscence, a finding consistent with our reported results for pullout force. Conversely, along the MV annulus, the linear relationship appears to be the reversed or nonexistent.

Taken together, the results of this additional analysis further underline structural differences between the two atrioventricular annuli. However, further studies dedicated toward identifying collagen alignment and crimp differences between the annuli are needed to confirm these hypotheses.